Inter-species cross-seeding: Stability and assembly of rat - Human amylin aggregates

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Berhanu, Workalemahu M ^a   Hansmann, Ulrich H E ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; OLIGOMER; PRAMLINTIDE; PROTEIN AGGREGATE;

ARTICLE; CONTROLLED STUDY; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN STABILITY; SPECIES COMPARISON; ANIMAL; CHEMISTRY; PROTEIN SECONDARY STRUCTURE; RAT; SPECIES DIFFERENCE;

ANIMALS; HUMANS; ISLET AMYLOID POLYPEPTIDE; MOLECULAR DYNAMICS SIMULATION; PROTEIN AGGREGATES; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RATS; SPECIES SPECIFICITY;

EID: 84901008858     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097051     Document Type: Article

References (82)

1. Blancas-Mejia LM, Ramirez-Alvarado M (2013) Systemic Amyloidoses. In: Kornberg RD, editor. Annual Review of Biochemistry, Vol 82. 745-774.
2. Lutz TA (2012) Control of energy homeostasis by amylin. Cellular and Molecular Life Sciences 69: 1947-1965.
3. Cao P, Marek P, Noor H, Patsalo V, Tu LH, et al. (2013) Islet amyloid: From fundamental biophysics to mechanisms of cytotoxicity. Febs Letters 587: 1106-1118.
4. Lorenzo A, Razzaboni B, Weir GC, Yankner BA (1994) Pancreatic-islet cell toxicity of amylin associated with type-2 diabetes-mellitus. Nature 368: 756-760. (Pubitemid 24153418)
5. Abedini A, Schmidt AM (2013) Mechanisms of islet amyloidosis toxicity in type 2 diabetes. Febs Letters 587: 1119-1127.
6. Brender JR, Salamekh S, Ramamoorthy A (2012) Membrane Disruption and Early Events in the Aggregation of the Diabetes Related Peptide IAPP from a Molecular Perspective. Accounts of Chemical Research 45: 454-462.
7. Gong W, Liu ZH, Zeng CH, Peng A, Chen HP, et al. (2007) Amylin deposition in the kidney of patients with diabetic nephropathy. Kidney International 72: 213-218. (Pubitemid 47067392)
8. Despa S, Margulies KB, Chen L, Knowlton AA, Havel PJ, et al. (2012) Hyperamylinemia Contributes to Cardiac Dysfunction in Obesity and Diabetes A Study in Humans and Rats. Circulation Research 110: 598-U224.
9. Jackson K, Barisone GA, Diaz E, Jin LW, DeCarli C, et al. (2013) Amylin Deposition in the Brain: A Second Amyloid in Alzheimer Disease? Annals of Neurology 74: 517-526.
10. Hartley DM, Walsh DM, Ye CPP, Diehl T, Vasquez S, et al. (1999) Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. Journal of Neuroscience 19: 8876-8884. (Pubitemid 30226709)
11. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, et al. (2005) The most infectious prion protein particles. Nature 437: 257-261. (Pubitemid 41294488)
12. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, et al. (2009) Fibril Fragmentation Enhances Amyloid Cytotoxicity. Journal of Biological Chemistry 284: 34272-34282.
13. Cremades N, Cohen SIA, Deas E, Abramov AY, Chen AY, et al. (2012) Direct Observation of the Interconversion of Normal and Toxic Forms of alpha-Synuclein. Cell 149: 1048-1059.
14. Sievers SA, Karanicolas J, Chang HW, Zhao A, Jiang L, et al. (2011) Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation. Nature 475: 96-U117.
15. Kabsch W, Sander C (1983) Dictionary of protein secondary structure - pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
16. Green J, Goldsbury C, Min T, Sunderji S, Frey P, et al. (2003) Full-length rat amylin forms fibrils following substitution of single residues from human amylin. Journal of Molecular Biology 326: 1147-1156. (Pubitemid 36263388)
17. Westermark P, Andersson A, Westermark GT (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiological Reviews 91: 795-826.
18. Middleton CT, Marek P, Cao P, Chiu CC, Singh S, et al. (2012) Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor. Nature Chemistry 4: 355-360.
19. Berhanu WM, Yasar F, Hansmann UH (2013) In Silico Cross Seeding of Abeta and Amylin Fibril-like Oligomers. ACS Chem Neurosci 4: 1488-1500.
20. Yoav Raz, Miller Y (2013) Interactions between Aβ and Mutated Tau Lead to Polymorphism and Induce Aggregation of Aβ-Mutated Tau Oligomeric Complexes. PLoS ONE 8: e73303.
21. Miller Y, Ma BY, Nussinov R (2011) Synergistic Interactions between Repeats in Tau Protein and A beta Amyloids May Be Responsible for Accelerated Aggregation via Polymorphic States. Biochemistry 50: 5172-5181.
22. Jaikaran E, Clark A (2001) Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochimica Et Biophysica Acta-Molecular Basis of Disease 1537: 179-203. (Pubitemid 33139801)
23. Kajava AV, Aebi U, Steven AC (2005) The parallel superpleated beta-structure as a model for amyloid fibrils of human amylin. Journal of Molecular Biology 348: 247-252. (Pubitemid 40462093)
24. Wiltzius JJW, Sievers SA, Sawaya MR, Cascio D, Popov D, et al. (2008) Atomic structure of the cross-beta spine of islet amyloid polypeptide (amylin). Protein Science 17: 1467-1474.
25. Luca S, Yau WM, Leapman R, Tycko R (2007) Peptide conformation and supramolecular organization in amylin fibrils: Constraints from solid-state NMR. Biochemistry 46: 13505-13522. (Pubitemid 350209947)
26. Bedrood S, Li YY, Isas JM, Hegde BG, Baxa U, et al. (2012) Fibril Structure of Human Islet Amyloid Polypeptide. Journal of Biological Chemistry 287: 5235-5241.
27. Härd T (2014) Amyloid Fibrils: Formation, Polymorphism, and Inhibition. J Phys Chem Lett 5 607-614.
28. Berhanu WM, Masunov AE (2013) Full length amylin oligomer aggregation: insight from molecular dynamic simulations and implications for design of aggregation inhibtors. Journal of Biomolecular Structure and Dynamics.
29. Xu WX, Su HB, Zhang JZH, Mu YG (2012) Molecular Dynamics Simulation Study on the Molecular Structures of the Amylin Fibril Models. Journal of Physical Chemistry B 116: 13991-13999.
30. Li YY, Hatmal MM, Langen R, Haworth IS (2012) Idealized Models of Protofilaments of Human Islet Amyloid Polypeptide. Journal of Chemical Information and Modeling 52: 2983-2991.
31. Smaoui MR, Poitevin F, Delarue M, Koehl P, Orland H, et al. (2013) Computational Assembly of Polymorphic Amyloid Fibrils Reveals Stable Aggregates. Biophysical Journal 104: 683-693.
32. Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, et al. (2013) Molecular Structure of beta-Amyloid Fibrils in Alzheimer's Disease Brain Tissue. Cell 154: 1257-1268.
33. Meyer V, Dinkel PD, Luo Y, Yu X, Wei G, et al. (2014) Single Mutations in Tau Modulate the Populations of Fibril Conformers through Seed Selection. Angew Chem Int Ed 53: 1590-1593.
34. Ma BY, Nussinov R (2012) Selective Molecular Recognition in Amyloid Growth and Transmission and Cross-Species Barriers. Journal of Molecular Biology 421: 172-184.
35. Kahler A, Sticht H, AHC H (2013) Conformational Stability of Fibrillar Amyloid-Beta Oligomers via Protofilament Pair Formation - A Systematic Computational Study. PLoS ONE 8: e70521.
36. Liang GZ, Zhao J, Yu X, Zheng J (2013) Comparative Molecular Dynamics Study of Human Islet Amyloid Polypeptide (IAPP) and Rat IAPP Oligomers. Biochemistry 52: 1089-1100.
37. Li Y, Xu WX, Mu YG, Zhang JZH (2013) Acidic pH retards the fibrillization of human islet amyloid polypeptide due to electrostatic repulsion of histidines. Journal of Chemical Physics 139.
38. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proceedings of the National Academy of Sciences of the United States of America 106: 14745-14750.
39. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, et al. (2006) Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins-Structure Function and Bioinformatics 65: 712-725. (Pubitemid 44583220)
40. Zachariae U, Schneider R, Briones R, Gattin Z, Demers JP, et al. (2012) beta-Barrel Mobility Underlies Closure of the Voltage-Dependent Anion Channel. Structure 20: 1540-1549.
41. Kutzner C, Grubmuller H, de Groot BL, Zachariae U (2011) Computational Electrophysiology: The Molecular Dynamics of Ion Channel Permeation and Selectivity in Atomistic Detail. Biophysical Journal 101: 809-817.
42. Pronk SPS, Roland Schulz R, Larsson P, Bjelkmar P, Apostolov R, et al. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Structural bioinformatics 29: 845-854.
43. Darden T, York D, Pedersen L (1993) Particle mesh ewald - an n. log(n) method for ewald sums in large systems. Journal of Chemical Physics 98: 10089-10092.
44. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh ewald method. Journal of Chemical Physics 103: 8577-8593.
45. Hess B (2008) P-LINCS: A parallel linear constraint solver for molecular simulation. Journal of Chemical Theory and Computation 4: 116-122.
46. Miyamoto S, Kollman PA (1992) Settle - an analytical version of the shake and rattle algorithm for rigid water models. Journal of Computational Chemistry 13: 952-962.
47. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. Journal of Chemical Physics 126.
48. Bussi G, Zykova-Timan T, Parrinello M (2009) Isothermal-isobaric molecular dynamics using stochastic velocity rescaling. Journal of Chemical Physics 130.
49. Parrinello M, Rahman A (1981) Polymorphic transitions in single-crystals - a new molecular-dynamics method. Journal of Applied Physics 52: 7182-7190. (Pubitemid 12456820)
50. DeLano WL (2002) PyMOL molecular graphics system. Version 1.3.0.4 Schrödinger, LLC.
51. Berhanu WM, Hansmann UHE (2013) The stability of cylindrin b-barrel amyloid oligomer models - A molecular dynamics study. Proteins: Structure, Function, and Bioinformatics 81.
52. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447: 453-457. (Pubitemid 46816731)
53. Tsemekhman K, Goldschmidt L, Eisenberg D, Baker D (2007) Cooperative hydrogen bonding in amyloid formation. Protein Science 16: 761-764. (Pubitemid 46507005)
54. Wiltzius JJW, Landau M, Nelson R, Sawaya MR, Apostol MI, et al. (2009) Molecular mechanisms for protein-encoded inheritance. Nature Structural & Molecular Biology 16: 973-U998.
55. Berhanu WM, Masunov AE (2012) Alternative packing modes as basis for amyloid polymorphismin five fragments. Peptide Science 98: 131-144.
56. Berhanu WM, Masunov AE (2011) Molecular dynamic simulation of wildtype and mutants of the polymorphic amyloid NNQNTF segments of elk prion: structural stability and thermodynamic of association. Biopolymers 95: 573-589.
57. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, et al. (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435: 773-778. (Pubitemid 40839722)
58. Berhanu WMM, AE (2012) Controlling the aggregation and rate of release in order to improve insulin formulation: molecular dynamics study of full-length insulin amyloid oligomer models. Journal of Molecular Modeling 18: 1129-1142.
59. Fox A, Snollaerts T, Casanova CE, Calciano A, Nogaj LA, et al. (2010) Selection for Nonamyloidogenic Mutants of Islet Amyloid Polypeptide (IAPP) Identifies an Extended Region for Amyloidogenicity. Biochemistry 49: 7783-7789.
60. Buchanan LE, Dunkelberger EB, Tran HQ, Cheng PN, Chiu CC, et al. (2013) Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient β-sheet. Proc Natl Acad Sci U S A 4: 19285-19290.
61. Bernhardt NA,WMB, Hansmann UHE (2013) Mutations and Seeding of Amylin Fibril-Like Oligomers. J Phys Chem B 117: 16076-16085.
62. Zhao J, Yu XA, Liang GZ, Zheng J (2011) Structural Polymorphism of Human Islet Amyloid Polypeptide (hIAPP) Oligomers Highlights the Importance of Interfacial Residue Interactions. Biomacromolecules 12: 210-220.
63. Wu C, Shea J-E (2013) Structural Similarities and Differences between Amyloidogenic and Non-Amyloidogenic Islet Amyloid Polypeptide (IAPP) Sequences and Implications for the Dual Physiological and Pathological Activities of These Peptides. PLoS Comput Biol 9: e1003211-1003223.
64. Milton NGN, Harris JR (2013) Fibril formation and toxicity of the non-amyloidogenic rat amylin peptide. Micron 44: 246-253.
65. Goldschmidt L, Teng PK, Riek R, Eisenberg D (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proceedings of the National Academy of Sciences of the United States of America 107: 3487-3492.
66. Spiliotopoulos D, Spitaleri A, Musco G (2012) Exploring PHD Fingers and H3K4me0 Interactions with Molecular Dynamics Simulations and Binding Free Energy Calculations: AIRE-PHD1, a Comparative Study. Plos One 7.
67. Kollman PA, Massova I, Reyes C, Kuhn B, Huo SH, et al. (2000) Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research 33: 889-897. (Pubitemid 32056774)
68. Caoa PAA, Wanga H, Tua LH, Zhanga X, Schmidtb AM, et al. (2013) Islet amyloid polypeptide toxicity and membrane interactions. Proc Natl Acad Sci USA.
69. Jang H, Connelly L, Arce FT, Ramachandran S, Kagan BL, et al. (2013) Mechanisms for the Insertion of Toxic, Fibril-like beta-Amyloid Oligomers into the Membrane. Journal of Chemical Theory and Computation 9: 822-833.
70. Poojari C, Xiao DQ, Batista VS, Strodel B (2013) Membrane Permeation Induced by Aggregates of Human Islet Amyloid Polypeptides. Biophysical Journal 105: 2323-2332.
71. Nanga RPR, Brender JR, Vivekanandan S, Ramamoorthy A (2011) Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment. Biochimica Et Biophysica Acta-Biomembranes 1808: 2337-2342.
72. Last NB, Miranker AD (2013) Common mechanism unites membrane poration by amyloid and antimicrobial peptides. Proceedings of the National Academy of Sciences of the United States of America 110: 6382-6387.
73. Jiang L, Liu C, Leibly D, Landau M, Zhao M, et al. (2013) Structure-based discovery of fiber-binding compounds that reduce the cytotoxicity of amyloid beta. Elife 2: e00857.
74. Zheng J, Jang H, Ma B, Tsai CJ, Nussinov R (2007) Modeling the Alzheimer A beta(17-42) fibril architecture: Tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophysical Journal 93: 3046-3057. (Pubitemid 350103369)
75. Quist A, Doudevski L, Lin H, Azimova R, Ng D, et al. (2005) Amyloid ion channels: A common structural link for protein-misfolding disease. Proceedings of the National Academy of Sciences of the United States of America 102: 10427-10432. (Pubitemid 41061570)
76. Poojari C, Strodel B (2013) Stability of Transmembrane Amyloid beta-Peptide and Membrane Integrity Tested by Molecular Modeling of Site-Specific A beta 42 Mutations. Plos One 8.
77. Nonoyama A, Laurence JS, Garriques L, Qi H, Le T, et al. (2008) A biophysical characterization of the peptide drug pramlintide (AC137) using empirical phase diagrams. Journal of Pharmaceutical Sciences 97: 2552-2567.
78. Chiu CC, Singh S, de Pablo JJ (2013) Effect of Proline Mutations on the Monomer Conformations of Amylin. Biophysical Journal 105: 1227-1235.
79. Apostol MI, Wiltzius JJW, Sawaya MR, Cascio D, Eisenberg D (2011) Atomic Structures Suggest Determinants of Transmission Barriers in Mammalian Prion Disease. Biochemistry 50: 2456-2463.
80. Fowler DM, Kelly JW (2012) Functional Amyloidogenesis and Cytotoxicity-Insights into Biology and Pathology. Plos Biology 10.
81. Seuring C, Greenwald J, Wasmer C, Wepf R, Saupe SJ, et al. (2012) The Mechanism of Toxicity in HET-S/HET-s Prion Incompatibility. Plos Biology 10.
82. Morales R, Moreno-Gonzalez I, Soto C (2013) Cross-Seeding of Misfolded Proteins: Implications for Etiology and Pathogenesis of Protein Misfolding Diseases. Plos Pathogens 9.